Entry Mode-Dependent Function of an Indole Glucosinolate Pathway in Arabidopsis for Nonhost Resistance against Anthracnose Pathogens

When faced with nonadapted fungal pathogens, Arabidopsis thaliana mounts nonhost resistance responses, which typically result in the termination of early pathogenesis steps. We report that nonadapted anthracnose fungi engage two alternative entry modes during pathogenesis on leaves: turgor-mediated...

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Bibliographic Details
Published in:The Plant cell 2010-07, Vol.22 (7), p.2429-2443
Main Authors: Hiruma, Kei, Onozawa-Komori, Mariko, Takahashi, Fumika, Asakura, Makoto, Bednarek, Paweł, Okuno, Tetsuro, Schulze-Lefert, Paul, Takano, Yoshitaka
Format: Article
Language:English
Subjects:
Appressoria
Arabidopsis - metabolism
Arabidopsis - microbiology
Arabidopsis thaliana
Biosynthesis
Colletotrichum
Colletotrichum gloeosporioides
Colletotrichum orbiculare
Conidia
Endocytosis
Fungi
Glucosinolates - metabolism
Host plants
Hyphae
Indoles - metabolism
Inoculation
Leaves
Lesions
Pathogens
Plant cells
Plant tissues
Plants
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Summary:When faced with nonadapted fungal pathogens, Arabidopsis thaliana mounts nonhost resistance responses, which typically result in the termination of early pathogenesis steps. We report that nonadapted anthracnose fungi engage two alternative entry modes during pathogenesis on leaves: turgor-mediated invasion beneath melanized appressoria, and a previously undiscovered hyphal tip-based entry (HTE) that is independent of appressorium formation. The frequency of HTE is positively regulated by carbohydrate nutrients and appears to be subject to constitutive inhibition by the fungal mitogen-activated protein kinase (MAPK) cascade of MAPK ESSENTIAL FOR APPRESSORIUM FORMATION1. The same MAPK cascade is essential for appressorium formation. Unexpectedly, the Arabidopsis indole glucosinolate pathway restricts entry of the nonadapted anthracnose fungi only when these pathogens employ HTE. Arabidopsis mutants defective in indole glucosinolate biosynthesis or metabolism support the initiation of postinvasion growth of nonadapted Colletotrichum gloeosporioides and Colletotrichum orbiculare. However, genetic disruption of Colletotrichum appressorium formation does not permit HTE on host plants. Thus, Colletotrichum appressoria play a critical role in the suppression of preinvasion plant defenses, in addition to their previously described role in turgor-mediated plant cell invasion. We also show that HTE is the predominant morphogenetic response of Colletotrichum at wound sites. This implies the existence of a fungal sensing system to trigger appropriate morphogenetic responses during pathogenesis at wound sites and on intact leaf tissue.
ISSN:1040-4651
1532-298X
DOI:10.1105/tpc.110.074344